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Levels of Selection:
Burying the Units-ofSelection Debate and
Unearthing the Crucial
New Issues
H. Kern Reeve and Laurent Keller
The purpose of this volume is to sample current theoretical and empirical
research on ( I) how natural selection among lower-level biological uni ts
(e.g., organisms) creates higher-level units (e.g., societies), and (2) given that
multiple levels exist, how natural selection at one biological level affects
selection at lower or higher levels. These two problems together constitute
what Leigh (chap. 2) caUs the "fundamental problem of ethology." Indeed,
as Leigh further suggests, they could be viewed jointly as the "fundamental
problem of biology," when genes and organisms are also included as adjacent levels in the biological hierarchy. This generalization has the desirable
property of immediately removing the long-slanding conceptual chasm between organismal and molecular biologist.<;.
These two problems are just beginning to be addressed, but their study
promises in the decades ahead to generate crucial insights (perhaps the crucial insight) into biological evolution both on our planet and on imagined
planets. To appreciate just how intriguingly intricate these problems are. we
use an analogy from particle physics to generate a heuristically useful picture of the myriad interlocking and concatenated selective forces acting simultaneously at different levels of biological organization (fig. 1.1). This
picture can be thought of as a visual guide to the kinds of multi level selection issues addressed in the chapters in this 'Volume.
First, however, we wish to make yet one more attempt to bury the issue
that usually usurps discussions of the levels of selection at the expense of the
truly interesting issues raised by these two problems; that is, the question of
what unit is the "true" fundamental unit of selection. This issue emerges in
cyclic debates about (a) whether genes or individuals are best seen as the
true units of selection, and (b) whether groups of individuals can be units of
selection. In our opinion, these questions have been satisfactorily answered
repeatedly, only to reappear subsequently with naive ferocity in new biological subdisciplines (e.g., the group-selection controversy is currently generating copious amounts of smoke within the human sciences; see, e.g., Wilson and
4 • REEVE AND KELLER
¥
10,~af
Burying the Debate over Whether Genes or Individuals
Are the Units of Selection
repUbive force
-
attractive force
./
centrifugal force
'-
0'
t
LEVELS OF SELECTION · 5
~O
r
O~ ~O
"
FIG. 1.1. The formation of higher-level vehicles from Iower-level vehides. A higher-level
vehicle forms when the attractive inclusive fitness force (see box 1.11 for Iower-levet
vehicles overcomes the repulsive and centrifugal inclusive fitfless forces.
Sober 1994 and responses; Sober and Wilson 1998). The particularly frustrating aspect of these constantly renewed debates is that, even though they
seemed to be sparked by rival theories about how evolution works, in fact,
they often involve only rival metaphors for the very same evolutionary logic
and are thus empirically empty.
Thus. we first pause to heap one more shovelful of dirt on the units-ofselection debates (a) and (b) above by very briefly reviewing what we
believe to be their well-established. correct (if not universally known) resolutions.
Organisms themselves are not replicated in the process of reproduction.
They die. and only their genes are passed on. This led Dawkins (1976. p. 12)
to propose that "the fundamental unit of selection. and therefore of selfinterest, is not the species, nor the group, nor even strictly. the individual. It
is the gene, the unit of heredity." Dawkins referred to this unil of self-interest as the replicator. or enduring unit of replication. Dawkins's view, which
builds on previous ideas by Hamilton (l964a) and Williams (19600), has
been criticized as too reductionist by those who argue that genes are not
directly visible to natural selection (e.g., Gould 1984; Sober and Lewontin
1984). That is, selection simply cannot pick among genes directly. but must
select among packages created by and containing these and other genes (e.g.,
organisms). Dawkins ( 1982), however, recognized organisms and perhaps
higher-level or laterally extended unilS as being vehicles, that is, Ihe units
directly confronting selection. We CXPCCI that. as the result of natural selection, vehicles will possess properties that maximize the replication success of
the sel of genes that cocremcd them . This picture is slightly modified by the
possibility of intragenomic selection (e.g., meiotic drive) favoring certain
genes. In this case, selection may seem to choose among genes directly.
However, a useful distinction still can be made between the replicator as a
piece of genetic information and the "vehicle" as the physical strelch of
DNA containing this genetic information. Thus. even in this case, it is only a
vehicle (albeit a replicalOr-/~vel vehicle) that directly confronts selection.
Thus, one internally consistent logical picture is that the unit of replication
is the gene (or, more precisely, the information contained in a gene), and the
organism is one kind of vehicle for suc h genes, a vehicle being the entity on
which selection aclS directly. The debate is resolved: Dawkins (1976) emphasized tha! genes (i.e., bilS of genetic information) are the enduring unilS
of replication, whereas Sober ( 1984) and Sober and Lewontin ( 1984) emphasized that individuals and possibly higher-level units, and not genes (as bilS
of genetic information), are vehicles. Case closed.
Burying the Old Group-Selection Debate
It is still embarassingly common to read inaccurate sllltemenlS in newspapers
and even in professional biological literature that frogs have to produce
many eggs to ensure the survival of the species because tadpoles suffer extremely high rates of predation. or that wolves have evolved ritualized displays to establish dominance hierarchies because physical combalS would be
6' REEVE AN D KEl L ER
too disadvantageous for the species. These naive statements beh'ay a widespread and persistent misunderstanding of the level at which natural selection most commonly operates.
Wynne-EcIwards (1962, 1993) has been the leading modem proponent of
the idea that animals behave for the good of the group. He suggested that a
population would become extinct if it overexploited its food resources; such
between-population selection has fixed population-level adaptations to prevent extinction (such as animal displays to signal population density and
thereby limit the risk of resource overexploitation). The most important criticism of this idea was formulated by Williams (l966a). Although selection at
the population level is theoretically possible, in practice, such selection will
be weak because of the high speed of within-population (between-individual) selection relative to that of between-population selection. Moreover, virtually all examples of group selection given by Wynne-Edwards (1962) have
been shown to be better understood with the individual-selection paradigm
(e.g., Alcock 1998; Kitchen and Packer, chap. 9). In Dawkins's terms, overwhelmingly strong theoretical arguments and empirical evidence tell us that
individuals, far more commonly than populations, are the vehicles.
More recently, formal models of within-population group selection-that
is, selection that occurs when a single breeding population is temporarily
broken up into subgroups within which both cooperative and competitive
actions can occur-have been developed under the rubric of "new group
selection," "intrademic group selection," or ''trait-group selection." These
models simply partition ordinary individual fitness into within- and betweengroup components-often using the clever covariance approach of Price
(1972)-and allow detailed predictions of the circumstances favoring the
evolution of traits affecting both within- and between-group fitness in various ways (e.g., Wilson 1975; Wilson and Sober 1989). These models are
mathematically equivalent to individual-selection (i.e., inclusive fitness)
models, however, and therefore do not point to a fundamentally different
kind of evolution (e.g., Dugatkin and Reeve 1994; Bourke and Franks 1995).
Thus, acknowledging the utility of these models should not be taken as a tiptoed retreat to Wynne-Edwardsian interpopulation selection, as is often mistakenly feared because of the shared label of "group selection." Acceptance
of these models also does not commit one to a particular view about the
relative baJance of cooperation and conflict in nature, because either can
have any degree of strength in these models (Dugalkin and Reeve 1994).
Furthermore, these models fit comfortably into Dawkins's (1982) conceptual
scheme because the "groups" in these models (e.g., animal societies) can be
viewed simply as vehicles above the level of the individual (Seeley 1997). A
distinct virtue of intrademic group-selection models is that they provide a
simple, s(atldardized means of unveiling the structure of selection working
simultaneously at different hierarchical levels (e.g., Dugatkin and Reeve
1994; Reeve and Keller 1997; Keller and Reeve, chap. 8).
LE VELS O F SEL ECTI ON· 7
Unearthing the New Issues
Most class lectures on levels of selection begin and end with a discussion of
the two (now stale) debates above. However, the current theoretical excitement in theoretical and empirical research in multileve1 selection centers on
the two problems set forth at the beginning of this introduction, namely, ( I)
how natural selection among lower-level biological vehicles creates higherlevel vehicles, and (2) given that multiple levels of vehicles exist, how natural selection at one level affects selection at lower or higher levels. The
richness of these two questions can be conveyed with the help of figure 1. 1,
which pictures interactio ns within and between lower- and higher-level vehicles (e.g., for vehicles ranging from single-celled organisms, to multicellular
individuals, to social groups of individuals).
An analogy from particle physics is useful here. Higher-level vehicles can
be seen as composites of lower-level vehicles, each of which experiences
both evolutionary repulsive (~) and attractive (>-<) bipolar forces with
other units at the same level (fig. 1.I). The separated unipolar forces can be
viewed as having magnitudes equal to the absolute inclusive fitnesses for
peaceful cooperation with a same-level partner unit (--<) or for competitive
suppression (e.g., killing) of the same partner unit (~). The outgoing arrows ( ? ) refer to the absolute inclusive fitness of a vehicle that leaves the
group; thus, this represents a second evolutionary force. which we call "centrifugal force," that tends to break apart the group. In this scheme, a cooperative group of lower-level units will be stable only if, for every unit, the
attractive force exceeds the maximum of the repulsive and centrifugal forces
also acting on that unit. (See box 1.1 for elaboration of the exact nature of
these forces.)
Figure 1.1 makes explicit several key features of the evolution of higherlevel vehicles from lower-level ones. First, a higher-level vehicle is created
from a lower~level vehicle whenever an attractive force arises that exceeds
both the maximal repUlsive and centrifugal forces. Interestingly, repulsive
forces among unbound lower-level units can create binding forces between
other such units, for example, as when ancestral multicellularity increased
the fused cells' ability to outcompete single-celled organisms for resources,
or when social grouping increased the ability of individuals to defend resources from intruding robbers.
Second, because the magnitude of each of the forces depends on inclusive
fitness, which in turn depends on both genetic relatedness and multiple ecologically determined costs and benefits of cooperation and noncooperation.' it
follows that understanding higher-level vehicle formation requ ires knowmg
both genetic and ecological factors that generate attractive, repulsive, and
centrifugal forces. Ecology will be crucially important in determining the
mal1nirude of the centrinl{l'1I1 fo~. hv ~tmnplv lIffl"r.tinp rhp. P.XnI'r.tM rf':nro-
8 • REEVE AND KELLER
BOX 1.1. THE ABSOLUTE INCLUSIVE
FITNESS "FORCE"
By absolule inclusive fitness. we mean a focal vehicle's direct reproductive
OUtpUI plus the sum, over all related vehicles, of the produCI of its relatedness
10 the vehicle times the reproductive OUtpul of that vehicle. Note that we use
absolute outputs, rather than changes in outputs caused by the focal vehicle
(the latter is used in most verbal fannulations of inclusive fitness). 1be outputs
of vehicles unaffected by the focal vehicle's actions will appropriately vanish
when the absolute inclusive fitnesses associated with the two actions by the
focal vehicle are compared by subtraction. because such outputs will have
exactly the same value in the compared inclusive fitnesses. For example, suppose a phenotype A causes the focal animal to have x offspring and a relative
(of relatedness r) 10 have y offspring. The corresponding offspring numbers for
phenotype B are z and w. The magnitudes of the corresponding absolute inclusive fitnesses (i.e., of the "forces") are
LEVElS OF SELECTION · 9
BOX 1.1. CONT.
(Grafen 1984, 1985). Condilionality of phenotypic expression can make these
assumptions more likely to bold (Parker 1989).
Our characterization of the magnitudes of the allractivc. repulsive, and centrifugal forces properly ties vehicle behavior to the interests of the ul timate
replicators, the genes that create the vehicles. Why? This scheme correctly
specifies when kin selection favors cooperation as summarized in Hamilton's
rule. That is, the sign of net inclusive fitness force determines whether kin
selection favors cooperation over killing or ejecting the partner and also over
leaving the group to reproduce independently. (The physical analogy breaks
down a bit here, because in the physical case, the net attractive force would
simply be the vector sum of all three forces, not the difference between the
attractive force and the maximum of the repulsive and centrifugal forces. Despite this, the physical picture is useful. )
x + ry
for A and
for B. The "net force" is then obtained by subtraction and is readily seen to
"'"~
(x - z)
+
r(y -
w),
which is the same as Hamilton's rule when set greater than zero (Grafen 1982,
1984, 1985). If action B did nOl change the reproductive output of the focal
individual's relative, then y = wand the term r(y - w) would simply vanish.
If the net force is greater than zero, phenotype A is favored.
The use of absolute offspring number in the above inclusive fitness calculations may sound wrong to some because of well-known theoretical admonitions agai nst (I) including personal offspring added because of help received
from others, and (2) giving inclusive fitness credit for the reprod uctive outputs
of relatives that are unaffected by the phenotype, both of which can cause
gross overestimation of the kin-selective value of a cooperative Strategy
(Grafen 1982, 1984). However, this is an error only when a strategy's absol ute
inclusive fitness is compared with zero, not when the absolute inclusive fitness
for one strategy is compared (by subtraction) with the absolute inclusive fitness
of another strategy. The latter procedure automatically yields the appropriate
description of net selective force by generating Hamilton's rule. It should be
mentioned., however, that the "absolute inclusive fitness force" approach is
precisely true only if there are additive costs and benefits and weak selection
ductive output of a dispersing, solitary vehicle. The most complete theories
of vehicle fonnation will thus be those that specify both the ecological and
the genetic contexts for vehicle creation.
Third, even if the creation of higher-level vehicles requires that attractive
forces exceed repulsive and centrifuga l forces, this does not imply that the
latter two forces will disappear o nce the higher- level vehicles are fonned.
They may continue to operate and shape the features of the higher-level
vehicle Gust as the confonnation of a stable molecule will depend o n the
internal electrical repuls ive forces). Indeed, repulsive forces may sometimes
strengthen sufficiently to cause subsequent vehicle breakdown. For example,
the attractive forces will often be sufficiently weak and variable that a composite vehicle lasts only a short time, just as an unstable, heavy particle
created in an particle accelerator may leave only a short track on a photographic plate before disintegrating into component particles. Analogously, in
many if not most animal species, the only cooperative groups are fleeting
associations of mates during courtship, copulation, and mate defense; that is,
the inclus ive fitness for cooperation (attractive force) exceeds that for noncooperation (repulsive and centrifugal forces) only until mating is completed.
A complete theory of social evolution will tell us not only the contexts in
which higher-level vehicles fonn, but also the c ontexts in which they break
down.
Finally, this model, represented in figure 1.1, predicts that larger cooperative groups are inherentl y less likely to be stable. Suppose there are n lowerlevel vehicles within the cooperative group (i.e., higher-level vehicle). U the
group is to be complete ly stable, the attractive forces must exceed the repu-
10 • REEVE AND KELLER
? RI
182
~
?A2
~t==+?Cl
FIG. 1.2. Major problems in understanding the evolution of higher-level vehicles. How do
attractive forces come to exceed repulsive and centrifugal forces lA 1 and A2.; see lexll?
How does the balance of these forces affect properties of the higher-level vehicle fB'
and B2; see text}? How does the interaction among forces within lower-level vehicles
affect the properties of the higher-level vehicle (Cl; see text)?
sive forces for all n(n -/) = n 2 - n polar interactions. and, in addition, the
attractive forces must exceed the centrifugal forces for all n cases, for a tOlal
of n 2 - n + n = n2 requirements. Thus, the number of Hamilton's rule
requirements for group slability increases as the square of the number of
group members! This immediately suggests that larger groups will be progressively less stable, unless high genetic relatedness, positive correlation
I FV ELS OF SELECTION · 11
:1Illong subunits in the values of their inclusive fitness parameters, or some
kind of between-subunit interaction somehow forces the multiple Hamilton's
mic requirements to be satisfied en masse. Furthermore, as lower-level vehides are nested to form higher-level vehicles, say from lower-level vehicles
consisting of nl subunits each to a higher-level vehicle of nh lower-level
vchicles, the total number of Hamilton 's rule requirements rapidly becomes
compounded to (nl'lh)l. This immediately suggests that vehicles created by
the nesting of successively higher-level vehicles will become progressively
less stable, again unless some condition or process causes these requirements
10 be satisfied at once.
Now we can represent the questions that together form the "fundamental
problem of biology," and thus the conceptual structure of this book, in terms
of the picture in figure 1.1. Questions A-C below refer to processes A-C in
figure 1.2.
Al. What attractive evolutionary forces bind low-level vehicles (i.e., vehicles nearly at the same level as the replic310rs themselves), like physical
stretches of DNA (replicators being the genetic information encoded in such
stretches), chromosomes. and cells, into intermediate-level vehicles, like
multicellular organisms? Under what conditions do these attractive forces
exceed the repulsive and centrifugal forces and under what conditions do
they not?
This topic is addressed in chapters 3 and 4. A central question in the study
of the origin of life is how cooperating groups of small replicator-Ievel vehicles could have arisen and how they could have prolecled themselves against
invasion by molecular parasites. Szathmary (chap. 3) argues that synergism
(i .e., division of labor and complementation of functions) provided the most
important attra<:tive force leading the first replicator-Ievel vehicles to associate. Cooperation was also facilitated by genetic compartmentalization that
resulled from limited dispersal and bonding of different replicator-level vehicles (which were therefore obliged to "sit in the same boat"; Szathmary,
chap. 3). Compartmentalization represented an important step in the overriding of repulsive and centrifugal forces and also probably led to their subsequent weakening. Finally, the benefits of division of labor. together with the
many advantages of larger size. were probably the two importanl attractive
forces that favored the transition from unicellular to multicellular life
(Michod, chap. 4).
A2. Similarly (as we move up the hierarchy of nested vehicles), what
attractive evolutionary forces bind intennediate-Ievel vehicles, such as organisms, into higher~ level vehicles, such as social groups of individuals?
Under what conditions do these attractive forces exceed the repulsive and
centrifugal forces?
This topic is addressed in chapters 5, 6, and 8-11. In sexual species, the
necessity of finding a mate provides an inescapable attractive force. In most
species, however, this attractive force is transient because males and females
r
12 • REEVE AND KELLER
typically have low genetic interest in each other's future (LesseIls. chap. 5).
Another attractive force may keep parents together: their common genetic
interest in rearing their offspring. The magrutude of this attractive force directly depends on the degree to which greater parental investment increases
offspring reproductive success (Godfray. chap. 6). This positive fon:e is opposed by the centrifugal force created by mating opportunities outside of the
pair bond. Thus, the dynamics of the attractive and centrifugal forces set the
stage for a variety of conflicts (new. subtle repulsive forces) between mates
over their relative investment in parentaJ care (LesselIs. chap. 5; Godfray.
chap. 6).
Attractive forces may also lead individuals other than mates to cooperate
when this increases either their survival or number of offspring produced or
the survival and fecundity of relatives. Higher relatedness increases the magnitude of the attractive forces and decreases the magnitude of the repulsive
forces (because increased relatedness between interacting individuals enhances the inclusive fitness payoffs for cooperation and reduces the inclusive
fitness payoffs for group-destructive selfishness). Increased relatedness thus
increases the scope both for reproductive altruism (whereby individuals
forgo direct reproduction to help others) and possibly for group stability.
although models of optimal reproductive skew (KelIer and Reeve, chap. 8)
predict that dominant members of animal societies may actually increase the
attractive force for potential subordinate helpers when the latter are less related. erasing any net effect of relatedness on group stability (Reeve and
Ratnieks 1993; Reeve 1998a). Not surprisingly, unreciprocated altruism occurs nearly exclusively in groups formed by closely related individuals (Keller and Reeve, chap. 8; Kitchen and Packer, chap. 9; Maynard Smith, chap.
10). Groups of unrelated individuals are generally stable only when group
living provides direct reproductive benefits to all group members. when it
requires no reproductive altruism, and opportunities for cheating are limited
(Le.• repUlsive forces are weakened) (Kitchen and Pack.er, chap. 9). The
other important factor shaping social life is the ability for individuals to
disperse successully and reproduce outside the group. Groups will be inherently more stable when such opportunities are limited (weak centrifugal
forces).
Interspeci.fic mutualism provides another interesting case of attractive
forces being stronger than repUlsive and centrifugal forces. the two forces
that generally predominate in interspecific interactions. Interestingly, the
same positive force (the benefits of division of labor) that facilitated the
evolution of early life is also probably important in shaping the nature of
interspecific cooperation (Heere. chap. 11). Moreover, Herre provides examples showing that stable interspecific cooperation (or reduced virulence) is
facilitated by the long-term association of interspecific individuals and parallel vertica1 transmission of the symbionts (from parents to offspring). The
consequence of symbionts being only vertically transmitted is similar to the
LEVELS OF SELECTION · 13
effect of compartmentalization of replicator-Ievel vehicles during the
early evolution of life because, in both cases, the imerests of replicators are
aligned. increasing the magnitude of the net attractive force.
Bt. How do attractive, repulsive. and centrifugal forces among lowerlevel vehicles interact to shape the properties of intermediate-level vehicles
like individuals'? Can differem repulsive forces sometimes nullify each other
within intermediate-Ievoel vehicles (as when there is some mechanism of policing against intragenomic selfishness) and thus leave an imprint on the characteristics of the intermediate-level vehicle (such as increased reproductive
efficiency resulting from greater internal cooperation)? Are there attractive
forces (perhaps arising omy after the creation of the intermediate-level vehicle) that would overcome all or some of the original repulsive forces and
thus leave an imprint OD the characteristics of the intermediate-level vehicle?
These topics are addressed in chaplers 4. 7, and 12. The two main forces
shaping the integrity of the organism are the attractive and repulsive forces
because lower-level vehicles (genes and cells) have little or no opportunity
to leave the organism and embark on independent and solitary lives (except
in some primitive multicellular organisms). The repulsive forces stem from
the benefits that lower-level vehicles (gene-level vehicles and cells) may
gain by increasing their reproductive rates at the expense of the other vehicles forming the organism. Thus. genes may increase their reproduction by
subverting meiosis in diploid organisms. Simi larly. cells may reap a shortterm reproductive benefit at the long-term expense of the organism through
uncontrolled cell proliferation (cancer). Michod (chap. 4) and Pomiankowksi
(chap. 7) provide examples of how repulsive forces can nullify each other to
decrease conflicts between genes and enforce fair meiosis. For example, it is
the mutual interest of genes in multicellular organisms in decreasing repulsive forces that probably led to the sequestration of a cell lineage set early in
development for the production of gametes (Michod, chap. 4). Mutual competition (repulsion) between cell lineages might result in no net advantage
for either, moreover, such competition might greatly limit the efficiency of
the vehicle formed by their cooperation. The separation of the germ line
reduced the opportunity for conflict (greatly reducing repulsive forces) and
thus was a first step toward the evolution of individuality (i.e.• a higher-level
vehicle with stronger attractive than repulsive forces). Similarly, because
most genes in the genome suffer from the detrimental effects of meioticdrive genes (unless linked with them), they are selectively favored to suppress the selfish actions of such genes (pomiankowski, chap. 7). Nunney
(chap. 12) suggests that between-lineage species selection may cause the
long-run predominance ef genetic architectures that decrease the risk of cancer (detrimental to the organism) and also that decrease the probability of a
shift from from sexual to asexual reproduction (the latter being deuimental
to the species). (Note that this is not Wynne-Edwardsian group selection,
becaure Nunnev 11; nnlv
~ne:lk inv
nf niffp.ll":ntilll
p.lrlin~tlnn
IImnnIJ !inp)lof';.<:
14' RE EVE AND KELLE R
that have different biological characteristics, the latter characteristics all having been fixed by within-population selection.) Under this intriguing view,
lineages with relatively high repulsive and low attractive forces (i.e.• those in
which lower-level vehicles are less likely to fonn higher-level vehicles) are
more likely to become extinct, leading to a long-tenn lineage selection for
c1ades that exhibit well-elaborated, high-level vehicles.
B2. Similarly, how do attractive, repulsive, and centrifugal forces interact
to shape the properties of h.igh-Ievel vehicles like animal societies? Can repulsive forces sometimes nullify each other within high-level vehicles (as in
policing against selfishness) and thus leave an imprint on the characteristics
of the high-level vehicle (such as increased efficiency resulting from greater
internal cooperation)? Are there attractive forces (perhaps originating only
after the initial creation of the high-level vehicle) that would nullify all or
some of the original repulsive forces and thus leave an imprint on the characteristics of the high-level vehicle?
These topics are addressed in chapters 8-1 1. For example, Keller and
Reeve (chap. 8) discuss how policing and bribing can promote inlragroup
cooperation within animal societies by in effect weakening repulsive forces
or strengthening attractive forces. Similarly, Maynard Smith (chap. 10) investigates the conditions favoring the emergence and enforcement of social
contract slrategies to punish selfish behaviors in human societies. Finally, the
evolution of co-adapted traits in obligately mutualistic species (e.g., figs and
their associates; Herre, chap. 11) provide yet another example of attractive
forces that arose or strengthened after the initial creation of a higher-level
vehicle from the mutualistic pair of organisms, that is, foDowing the evolution of complete reproductive interdependence.
Cl. Perhaps the most unexplored question concerns how interactions between lower-level vehicles might affect the interactions between intennediate-level vehicles and thus affect the properties of the higbest-Ievel vehicle.
For example, Keller and Reeve (chap. 8) describe one of Reeve's ( 1998b)
hypotheses for the absence of nepotism within insect societies. Intragenomic
selection on parentally imprinted alleles involved in kin recognition Oowestlevel vehicles) might favor sabotaging of the potential nepltism-dispensing
machinery of individuals (intennediate-Ievel vehicles), leading to the lack of
nepotism and thus increased cooperation within hymenopteran societies
(highest-level vehicles).
Acknowledgments
We thank E. Leigh for useful comments on the manuscript. We were supported by grants from the Swiss and U.S. NSF.
2
Levels of Selection,
Potential Conflicts, and
Their Resolution: The
Role of the "Com mon
Good"
Egbert Giles Leigh, Jr.
I
Adaptation is shaped by the competitive process of natural selection (Darwin
1859). Genes are the units whose "self-interest" drives natural selection. In
other words, nothing nonrandom happens in the evolution of a species unless
it "serves the self-interest"' -causes the differential reproduction-of some
gene (Dawkins 1976; Bourke and Franks 1995). Yet no one of these genes,
ultimate unit of self-interest though it might be, can do a thing outside the
context provided by the rest of its genome and the organism for which that
genome is appropriate. Alone, a gene is as useless as a fragment of a computer program without the rest of the program, a computer suited to run the
program, and an operator capable of using the program and the machine. In
short, the units of competitive self-interest that make up a genome are unerly
interdependent.. How did the competitive process of natural selection shape
so intricate a mutualism?
Ecological communities are structured to a large extent by competition:
competition among individuals for food or space, and competition between
consumers and their potential prey over who uses the resources in these
prey's bodies (Hutchinson 1959; Paine 1966). Competition among plants for
light, water, and nutrients, and between consumers and their intended prey, is
particularly intense in tropical forest (Robinson 1985; Richards 1996). Yet
tropical forest is not only a climax of competition but an apex of mutualism.
Plants depend on fungi for the uptake of nutrients (Alien 1991) and on ani~
mals for pollination of their Howers, dispersal of their seeds, sometimes for burial of their seeds out of the reach of insect pests (Corner 1964;
Smythe 1989; Forget 1991 ). These mutualisms make possible the diversity
and luxuriance of tropical forest (Corner 1964; Regal 1977; Crepet 1984).
They constitute an extraordinary web of interdependence. A tree species that
needs agoutis to bury its seeds needs other tree species to keep the agoutis
fed when it itself is not fruiting (Forget 1994). The durian whose flowers are
pollinated by bats needs mangroves to keep these bats in nectar when the
durian's forest has few plants in Hower (Lee 1980). Although ecological